A considerable part of the diversity of eukaryotic phototrophs consists of algae with plastids that evolved from endosymbioses between two eukaryotes. These complex plastids are characterized by a high number of envelope membranes (more than two) and some of them contain a residual nucleus of the endosymbiotic alga called a nucleomorph. Complex plastid-bearing algae are thus chimeric cell assemblies, eukaryotic symbionts living in a eukaryotic host. In contrast, the primary plastids of the Archaeplastida (plants, green algae, red algae, and glaucophytes) possibly evolved from a single endosymbiosis with a cyanobacterium and are surrounded by two membranes. Complex plastids have been acquired several times by unrelated groups of eukaryotic heterotrophic hosts, suggesting that complex plastids are somewhat easier to obtain than primary plastids. Evidence suggests that complex plastids arose twice independently in the green lineage (euglenophytes and chlorarachniophytes) through secondary endosymbiosis, and four times in the red lineage, first through secondary endosymbiosis in cryptophytes, then by higher-order events in stramenopiles, alveolates, and haptophytes. Engulfment of primary and complex plastid-containing algae by eukaryotic hosts (secondary, tertiary, and higher-order endosymbioses) is also responsible for numerous plastid replacements in dinoflagellates. Plastid endosymbiosis is accompanied by massive gene transfer from the endosymbiont to the host nucleus and cell adaptation of both endosymbiotic partners, which is related to the trophic switch to phototrophy and loss of autonomy of the endosymbiont. Such a process is essential for the metabolic integration and division control of the endosymbiont in the host. Although photosynthesis is the main advantage of acquiring plastids, loss of photosynthesis often occurs in algae with complex plastids. This chapter summarizes the essential knowledge of the acquisition, evolution, and function of complex plastids.

• Keywords
• Complex endosymbiosis, Plastid replacement, Reductive evolution,
• MeSH
• Biological Evolution * MeSH
• Phylogeny MeSH
• Plastids genetics   metabolism   MeSH
• Rhodophyta * genetics   MeSH
• Plants genetics   MeSH
• Symbiosis MeSH
• Publication type
• Journal Article MeSH

Fatty acids are essential components of biological membranes, important for the maintenance of cellular structures, especially in organisms with complex life cycles like protozoan parasites. Apicomplexans are obligate parasites responsible for various deadly diseases of humans and livestock. We analyzed the fatty acids produced by the closest phototrophic relatives of parasitic apicomplexans, the chromerids Chromera velia and Vitrella brassicaformis, and investigated the genes coding for enzymes involved in fatty acids biosynthesis in chromerids, in comparison to their parasitic relatives. Based on evidence from genomic and metabolomic data, we propose a model of fatty acid synthesis in chromerids: the plastid-localized FAS-II pathway is responsible for the de novo synthesis of fatty acids reaching the maximum length of 18 carbon units. Short saturated fatty acids (C14:0-C18:0) originate from the plastid are then elongated and desaturated in the cytosol and the endoplasmic reticulum. We identified giant FAS I-like multi-modular enzymes in both chromerids, which seem to be involved in polyketide synthesis and fatty acid elongation. This full-scale description of the biosynthesis of fatty acids and their derivatives provides important insights into the reductive evolutionary transition of a phototropic algal ancestor to obligate parasites.

• Keywords
• Chromera velia, Vitrella brassicaformis, de novo biosynthesis, desaturation, elongation, evolution, fatty acids,
• MeSH
• Apicomplexa classification   genetics   metabolism   MeSH
• Biosynthetic Pathways genetics   MeSH
• Fatty Acid Desaturases classification   genetics   metabolism   MeSH
• Species Specificity MeSH
• Fatty Acid Elongases classification   genetics   metabolism   MeSH
• Phylogeny MeSH
• Humans MeSH
• Fatty Acids biosynthesis   MeSH
• Evolution, Molecular MeSH
• Protozoan Infections parasitology   MeSH
• Protozoan Proteins classification   genetics   metabolism   MeSH
• Fatty Acid Synthase, Type II classification   genetics   metabolism   MeSH
• Fatty Acid Synthase, Type I classification   genetics   metabolism   MeSH
• Animals MeSH
• Check Tag
• Humans MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Fatty Acid Desaturases MeSH
• Fatty Acid Elongases MeSH
• Fatty Acids MeSH
• Protozoan Proteins MeSH
• Fatty Acid Synthase, Type II MeSH
• Fatty Acid Synthase, Type I MeSH

Aminoacyl-tRNA synthetases (AaRSs) are enzymes that catalyze the ligation of tRNAs to amino acids. There are AaRSs specific for each amino acid in the cell. Each cellular compartment in which translation takes place (the cytosol, mitochondria, and plastids in most cases), needs the full set of AaRSs; however, individual AaRSs can function in multiple compartments due to dual (or even multiple) targeting of nuclear-encoded proteins to various destinations in the cell. We searched the genomes of the chromerids, Chromera velia and Vitrella brassicaformis, for AaRS genes: 48 genes encoding AaRSs were identified in C. velia, while only 39 AaRS genes were found in V. brassicaformis. In the latter alga, ArgRS and GluRS were each encoded by a single gene occurring in a single copy; only PheRS was found in three genes, while the remaining AaRSs were encoded by two genes. In contrast, there were nine cases for which C. velia contained three genes of a given AaRS (45% of the AaRSs), all of them representing duplicated genes, except AsnRS and PheRS, which are more likely pseudoparalogs (acquired via horizontal or endosymbiotic gene transfer). Targeting predictions indicated that AaRSs are not (or not exclusively), in most cases, used in the cellular compartment from which their gene originates. The molecular phylogenies of the AaRSs are variable between the specific types, and similar between the two investigated chromerids. While genes with eukaryotic origin are more frequently retained, there is no clear pattern of orthologous pairs between C. velia and V. brassicaformis.

• Keywords
• Aminoacyl tRNA synthetase (AaRS), Chromera velia, Vitrella brassicaformis, chloroplast, evolution, mitochondrion, nucleus, protein localization,
• MeSH
• Alveolata classification   enzymology   genetics   MeSH
• Amino Acyl-tRNA Synthetases genetics   MeSH
• Phylogeny MeSH
• Protozoan Proteins genetics   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Amino Acyl-tRNA Synthetases MeSH
• Protozoan Proteins MeSH

Photosynthesis is a biochemical process essential for life, serving as the ultimate source of chemical energy for phototrophic and heterotrophic life forms. Since the machinery of the photosynthetic electron transport chain is quite complex and is unlikely to have evolved multiple independent times, it is believed that this machinery has been transferred to diverse eukaryotic organisms by endosymbiotic events involving a eukaryotic host and a phototrophic endosymbiont. Thus, photoautotrophy, as a benefit, is transmitted through the evolution of plastids. However, many eukaryotes became secondarily heterotrophic, reverting to hetero-osmotrophy, phagotrophy, or parasitism. Here, I briefly review the constructive evolution of plastid endosymbioses and the consequential switch to reductive evolution involving losses of photosynthesis and plastids and the evolution of parasitism from a photosynthetic ancestor.

• Keywords
• endosymbiosis, evolution, parasitism, phagotrophy, photosynthesis, plastid, secondary heterotrophy,
• MeSH
• Chlorophyta * metabolism   microbiology   MeSH
• Heterotrophic Processes MeSH
• Symbiosis * MeSH
• Electron Transport MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Review MeSH

Endosymbioses necessitate functional cooperation of cellular compartments to avoid pathway redundancy and streamline the control of biological processes. To gain insight into the metabolic compartmentation in chromerids, phototrophic relatives to apicomplexan parasites, we prepared a reference set of proteins probably localized to mitochondria, cytosol, and the plastid, taking advantage of available genomic and transcriptomic data. Training of prediction algorithms with the reference set now allows a genome-wide analysis of protein localization in Chromera velia and Vitrella brassicaformis. We confirm that the chromerid plastids house enzymatic pathways needed for their maintenance and photosynthetic activity, but for carbon and nitrogen allocation, metabolite exchange is necessary with the cytosol and mitochondria. This indeed suggests that the regulatory mechanisms operate in the cytosol to control carbon metabolism based on the availability of both light and nutrients. We discuss that this arrangement is largely shared with apicomplexans and dinoflagellates, possibly stemming from a common ancestral metabolic architecture, and supports the mixotrophy of the chromerid algae.

• Keywords
• chromerid, endosymbiosis, mixotrophy, plastid integration, prediction algorithm, protein localization,
• MeSH
• Algorithms MeSH
• Alveolata metabolism   MeSH
• Cytosol metabolism   MeSH
• Nitrogen metabolism   MeSH
• Photosynthesis genetics   physiology   MeSH
• Phylogeny MeSH
• Evolution, Molecular MeSH
• Symbiosis genetics   physiology   MeSH
• Carbon metabolism   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Nitrogen MeSH
• Carbon MeSH

In oxygenic photosynthesis the initial photochemical processes are carried out by photosystem I (PSI) and II (PSII). Although subunit composition varies between cyanobacterial and plastid photosystems, the core structures of PSI and PSII are conserved throughout photosynthetic eukaryotes. So far, the photosynthetic complexes have been characterised in only a small number of organisms. We performed in silico and biochemical studies to explore the organization and evolution of the photosynthetic apparatus in the chromerids Chromera velia and Vitrella brassicaformis, autotrophic relatives of apicomplexans. We catalogued the presence and location of genes coding for conserved subunits of the photosystems as well as cytochrome b6f and ATP synthase in chromerids and other phototrophs and performed a phylogenetic analysis. We then characterised the photosynthetic complexes of Chromera and Vitrella using 2D gels combined with mass-spectrometry and further analysed the purified Chromera PSI. Our data suggest that the photosynthetic apparatus of chromerids underwent unique structural changes. Both photosystems (as well as cytochrome b6f and ATP synthase) lost several canonical subunits, while PSI gained one superoxide dismutase (Vitrella) or two superoxide dismutases and several unknown proteins (Chromera) as new regular subunits. We discuss these results in light of the extraordinarily efficient photosynthetic processes described in Chromera.

• MeSH
• Alveolata genetics   physiology   MeSH
• Gene Deletion MeSH
• Photosynthesis genetics   physiology   MeSH
• Photosystem I Protein Complex genetics   isolation & purification   physiology   MeSH
• Phylogeny MeSH
• Mass Spectrometry MeSH
• Evolution, Molecular MeSH
• Superoxide Dismutase metabolism   MeSH
• Thylakoids metabolism   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Photosystem I Protein Complex MeSH
• Superoxide Dismutase MeSH

Most photosynthetic eukaryotes synthesize both heme and chlorophyll via a common tetrapyrrole biosynthetic pathway starting from glutamate. This pathway was derived mainly from cyanobacterial predecessor of the plastid and differs from the heme synthesis of the plastid-lacking eukaryotes. Here, we show that the coral-associated alveolate Chromera velia, the closest known photosynthetic relative to Apicomplexa, possesses a tetrapyrrole pathway that is homologous to the unusual pathway of apicomplexan parasites. We also demonstrate that, unlike other eukaryotic phototrophs, Chromera synthesizes chlorophyll from glycine and succinyl-CoA rather than glutamate. Our data shed light on the evolution of the heme biosynthesis in parasitic Apicomplexa and photosynthesis-related biochemical processes in their ancestors.

• MeSH
• Acyl Coenzyme A metabolism   MeSH
• Alveolata metabolism   MeSH
• Chlorophyll biosynthesis   MeSH
• Photosynthesis * MeSH
• Phylogeny MeSH
• Glycine metabolism   MeSH
• Molecular Sequence Data MeSH
• DNA, Protozoan genetics   MeSH
• Sequence Analysis, DNA MeSH
• Tetrapyrroles biosynthesis   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Acyl Coenzyme A MeSH
• Chlorophyll MeSH
• Glycine MeSH
• DNA, Protozoan MeSH
• succinyl-coenzyme A MeSH Browser
• Tetrapyrroles MeSH

Genes encoding enzymes of the tetrapyrrole biosynthetic pathway were searched within Euglena gracilis EST databases and 454 genome reads and their 5' end regions were sequenced when not available. Phylogenetic analyses and protein localization predictions support the hypothesis concerning the presence of two separated tetrapyrrole pathways in E. gracilis. One of these pathways resembles the heme synthesis in primarily heterotrophic eukaryotes and was presumably present in the host cell prior to secondary endosymbiosis with a green alga. The second pathway is similar to the plastid-localized tetrapyrrole syntheses in plants and photosynthetic algae. It appears to be localized to the secondary plastid, presumably derived from an algal endosymbiont and probably serves only for the production of plastidial heme and chlorophyll. Thus, E. gracilis represents an evolutionary intermediate in a metabolic transformation of a primary heterotroph to a photoautotroph through secondary endosymbiosis. We propose here that the tetrapyrrole pathway serves as a highly informative marker for the evolution of plastids and plays a crucial role in the loss of plastids.

• MeSH
• Biological Evolution * MeSH
• Biosynthetic Pathways * MeSH
• Chlorophyta physiology   MeSH
• Euglena gracilis classification   genetics   physiology   MeSH
• Phylogeny MeSH
• Molecular Sequence Data MeSH
• Plastids genetics   metabolism   MeSH
• Protozoan Proteins genetics   metabolism   MeSH
• Symbiosis MeSH
• Tetrapyrroles biosynthesis   MeSH
• Publication type
• Letter MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Protozoan Proteins MeSH
• Tetrapyrroles MeSH

BACKGROUND: The endosymbiotic birth of organelles is accompanied by massive transfer of endosymbiont genes to the eukaryotic host nucleus. In the centric diatom Thalassiosira pseudonana the Psb28 protein is encoded in the plastid genome while a second version is nuclear-encoded and possesses a bipartite N-terminal presequence necessary to target the protein into the diatom complex plastid. Thus it can represent a gene captured during endosymbiotic gene transfer. METHODOLOGY/PRINCIPAL FINDINGS: To specify the origin of nuclear- and plastid-encoded Psb28 in T. pseudonana we have performed extensive phylogenetic analyses of both mentioned genes. We have also experimentally tested the intracellular location of the nuclear-encoded Psb28 protein (nuPsb28) through transformation of the diatom Phaeodactylum tricornutum with the gene in question fused to EYFP. CONCLUSIONS/SIGNIFICANCE: We show here that both versions of the psb28 gene in T. pseudonana are transcribed. We also provide experimental evidence for successful targeting of the nuPsb28 fused with EYFP to the diatom complex plastid. Extensive phylogenetic analyses demonstrate that nucleotide composition of the analyzed genes deeply influences the tree topology and that appropriate methods designed to deal with a compositional bias of the sequences and the long branch attraction artefact (LBA) need to be used to overcome this obstacle. We propose that nuclear psb28 in T. pseudonana is a duplicate of a plastid localized version, and that it has been transferred from its endosymbiont.

• MeSH
• Cell Nucleus genetics   MeSH
• Molecular Sequence Data MeSH
• Plastids genetics   MeSH
• Proteins chemistry   genetics   MeSH
• Diatoms genetics   MeSH
• Amino Acid Sequence MeSH
• Sequence Homology, Amino Acid MeSH
• Symbiosis genetics   MeSH
• Gene Transfer Techniques MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Proteins MeSH

The majority of eukaryotic diversity is hidden in protists, yet our current knowledge of processes and structures in the eukaryotic cell is almost exclusively derived from multicellular organisms. The increasing sensitivity of molecular methods and growing interest in microeukaryotes has only recently demonstrated that many features so far considered to be universal for eukaryotes actually exist in strikingly different versions. In other words, during their long evolutionary histories, protists have solved general biological problems in many more ways than previously appreciated. Interestingly, some groups have broken more rules than others, and the Euglenozoa and the Alveolata stand out in this respect. A review of the numerous odd features in these 2 groups allows us to draw attention to the high level of convergent evolution in protists, which perhaps reflects the limits that certain features can be altered. Moreover, the appearance of one deviation in an ancestor can constrain the set of possible downstream deviations in its descendents, so features that might be independent functionally, can still be evolutionarily linked. What functional advantage may be conferred by the excessive complexity of euglenozoan and alveolate gene expression, organellar genome structure, and RNA editing and processing has been thoroughly debated, but we suggest these are more likely the products of constructive neutral evolution, and as such do not necessarily confer any selective advantage at all.

• MeSH
• Dinoflagellida physiology   MeSH
• Euglenida physiology   MeSH
• Phylogeny * MeSH
• Adaptation, Physiological physiology   MeSH
• Evolution, Molecular * MeSH
• Genes, Protozoan physiology   MeSH
• Gene Expression Regulation physiology   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH